Rapid GIS-based profiling of West Nile virus transmission: defining environmental factors associated with an urban-suburban outbreak in Northeast Ohio, USA

Abstract

Human West Nile virus (WNV) infection was first detected in Cuyahoga county, Ohio, USA, in 2002. During that year's extensive epidemic/epizootic among non-immune human and bird populations, the county experienced 155 cases of severe human West Nile neurological disease (WNND, incidence = 11.1 cases/100,000), with 11 fatalities. Structured serosurveys indicated that 1.9%, or approximately 26,000 of county residents (population = 1,372,303) were infected that year. In early 2003, in order to better focus monitoring and control efforts, we used a geographical information system (GIS) approach and spatial statistical analysis to identify the association of environmental factors and human population structure with the observed local risk for WNV transmission. Within the varied range of urban/suburban/ rural habitats across the 1186 km2 county, exploratory analysis indicated significant clustering of WNND risk in inner-ring suburbs. Subsequent discriminant factor analysis based on inputs of census and land-use/land cover data was found to effectively classify sub-areas of the county having low, medium and high WNV risk. On a 1036 ha quadrat scale of resolution, higher risk of human infection was significantly associated with higher-income areas, increased fractionation of habitat and older housing, while it was negatively associated with areas of agricultural land, wetland or forest. The areal classification of WNV transmission risk has been validated over time through detection of increased local Culex spp. mosquito density (2002-2006), and increased frequency of WNV positive mosquito pools within the medium- and high-risk quadrats. This timely working identification of the transmission scale effectively focused control interventions against newly invasive WNV in a complex North American habitat.

Figure 1

Upper panel, distribution of severe human WNV-associated neurological disease (WNND) cases by residence location in Cuyahoga County, 2002. For this map, black outlines indicate boundaries of individual cities and municipal townships included within the county limits; Lower panel, local age-adjusted attack rates for WNND within established US Government census tracts of Cuyahoga County. Increased age-adjusted risk is indicated by darker shades of color. For the county at-large, the 2002 rate of WNND was 16 per 100,000 population.

Figure 2

Cuyahoga County census tract locations showing significant local clustering of high WNND incidence for 2002 within southern and western Cleveland and its inner ring suburbs in the west, southwest, and east. Rings indicate significant population-adjusted case clustering by Besag-Newell scan statistic.

Figure 3

Topographic and Land use/ Land cover characteristics of Cuyahoga County. Upper panel, elevation map of the county, showing altitude above mean Lake Erie shoreline level. Higher altitudes in the east and south drain toward the lake to the north and west. Black outlines indicate the chosen analytic quadrat grid used in data aggregation for discriminant analysis of WNV risk; Lower panel, Land use classification of Cuyahoga County and surrounding areas. The central county is predominantly urban (magenta and pink) surrounded at the periphery by open agricultural and parkland, including forested and wetland areas.

Figure 4

Examples of GIS data inputs for risk modeling. Upper panel, All Cuyahoga County roads in purple, with analytic quadrat grid overlaid in black; Lower panel, location of older housing stock as determined by census tract for year 2000 US census data on age of individual domiciliary structures.

Figure 5

Identified high-, medium-, and low-risk areas for human WNV infection within Cuyahoga County in 2002, based on discriminant analysis of environmental and population features derived from US census and land-use/ land-cover databases (see Figures 3 and 4). Green circles indicate approximate residence locations of 2002 human WNND cases.

Figure 6

Observed variation in mosquito trap outcomes according to grid area classification for WNV risk. Upper panel, Median mosquito numbers recovered per gravid trap night in high-, moderate-, and low-risk grid areas; Lower panel, percentage of per trap mosquito pools that tested positive for WNV each month in the stratified grid risk areas between May 2002 and September 2006.

Figure 7

Mean monthly temperatures in Cuyahoga County, Ohio (red line), showing two periods of anomalous warm winter temperatures in 1974–75 (green line), and in 2001–2002 (blue line). The 1974–75 event was associated with an outbreak of St. Louis Encephalitis (SLE) virus-related disease. The 2001–2002 event was associated with the County’s first WNV epidemic.